Following the Fall of Beacon, Team RWBY was scattered by the battle; with every member going into their separate ways. Without Ozpin to guide them, Ruby Rose and the remaining members of Team JNPR formed Team RNJR to travel to Mistral in order to bring justice to Cinder's Faction for attacking Beacon.
During their travels, Qrow Branwen followed RNJR, unbeknownst to them, protecting the team from any Grimm along the way. Qrow made himself known to the team when RNJR was attacked by Tyrian Callows, who had been sent to capture Ruby under Salem's orders. Qrow defeats Tyrian, but is poisoned by the Faunus' stinger, leading the group to rush to Mistral, stopping to face the Nuckelavee in the abandoned settlement of Kuroyuri, where they were rescued by the Mistral police force.
The group is later ambushed by Leo and Salem's forces in Haven, who planned to steal the Relic of Knowledge from the Academy in order to complete their goals. In the ensuing battle, the White Fang are cornered and defeated by Blake Belladonna and the Menagerie Faunas militia, while Leo, Emerald, Mercury, and Hazel are forced to retreat by Ruby's Group. Meanwhile at the vault, Yang discovered Raven was the true Spring Maiden, and convinces her to not take the Relic, preventing the Fall of Haven. The group then plans to take the Relic to Altas, with Blake joining them.
Two weeks later, the group attempted to travel to Argus in order to secure the Relic in Atlas, but were forced to briefly separate into two groups due to a train crash, where RWBY, Qrow, and Oscar were left behind and forced to hike to the city, meeting Maria Calavera in the process. There, the group discovered the truth about Ozpin and Salem through Jinn's recounting of their past, which led to Ozpin sealing himself away deep in Oscar's mind. The group takes shelter from a snowstorm at Brunswick Farms, where they debate going to Atlas, now that they know Salem is immortal. However, after a close encounter with a pack of Apathy, the group continue on their journey.
Team JNR stayed with Jaune's sister Saphron and her wife while waiting for Team RWBY's group to arrive. The Arc House served as a temporary base for the group while they attempted to find a way to Atlas.
Due to Caroline Cordovin being unwilling to let the group take an airship to Atlas, the group was forced to steal one and fight Cordovin's Colossus while Blake and Yang fought against Adam Taurus. The group manages to defeat both of them, but unfortunately a Leviathan arrives with an army of Grimm to destroy Argus. Ruby, with the assistance of Jinn, is able to stop the Grimm with her Sliver Eyes. As thanks for saving the city, Cordovin allows the group to leave, promising she won’t mention them in her report.
The newfound Huntsmen proceed to go on various missions and train at Atlas Academy.
During Robyn Hill's election party Tyrian attacks the people and Arthur Watts hacks the video framing Penny. The event causes Grimm to attack Mantle forcing Ruby's Group and the Ace-Ops to fight into the night defending the city.
During the group's visit of the Schnee Manor. Weiss found out that Jacques Schnee allied himself with Watts and exposes her father to Ironwood and the Altas council, and Jacques is arrested.
Watts uses his credentials to disable Mantle's heat causing discord and panic and Ruby's Group is sent with the Ace-Ops to deal with the Grimm invasion. The panic is slightly released when Ironwood reveals the truth about the Grimm and Salem to the people.
However, Team RWBY and the Ace-Ops are later called back to Atlas Academy by Ironwood while Jaune, Ren, and Nora go off to find Oscar. Ironwood breaks down after realizing Cinder has infiltrated the school and confronts the groups on the lies they told him. A Seer then pops out of Watts's bag and dies, causing Salem to manifest from it to inform them she is on her way. Ironwood decides the best plan to keep the Relics from her reach is to use the Relic of Creation to raise Atlas, abandoning Mantle, much to Team RWBY's horror and anger.
Now seeing the girls as enemies, he declares them, JNR, Oscar, and Qrow as wanted criminals to be detained on sight and officially cuts his ties with them. Team RWBY manages to defeat the Ace-Ops and get help from Pietro and Maria to escape the school. To make matters worse Neopolitan, (who Cinder bought along to Atlas) steals the lamp from Team ONNJ. Ruby and Weiss go to the Winter Maiden and find Winter and Penny fighting with Cinder over the Maiden's powers. Ruby uses her Silver Eyes to stop Cinder's relentless attack, forcing her to flee while Penny, the new Maiden, goes with Ruby and the others. However, the group sees a massive swarm of Grimm led by Salem herself.
After recovering Oscar from the Crater slums underneath Atlas, the group reunited in a restaurant in Mantle to discuss their next move and see their wanted post from Atlas news broadcast. Ruby decided they need to turn on Amity Communications Tower to warn Remnant about Salem, however Yang disagrees and instead want to evacuate and protect the Mantle citizens due to several problems with it. As a result of a suggestion by Jaune and Oscar, the group splits in two to tackle both problems. Lately, the group recorded a broadcast for Ruby's message to Remnant. As the group gets ready to return to Atlas, Ironwood calls Penny in an attempt to have her return but ended the call after Ruby failed to convince him to save Mantle.
The group along with Penny and May Marigold arrives at Snow Shoe Shipping Facility which is owned by the Schnee Dust Company. Weiss then figured out which tube they will take to reach Atlas, where she's comically launched by Nora up to Atlas. Upon reaching Atlas, May Marigold use her Semblance to help the group and Penny sneak through the Atlas Military compound to reach Ironwood's terminal. Once they arrive at the terminal, through Pietro Polendina, Penny obtains the access codes needed to launch Amity Tower once Penny reaches it. The group is then ambushed by the Ace Operatives, which results in a brief battle where the group is able to escape Atlas. However, Nora is critically injured after using her Semblance to break open a locked door, while the Ace Ops steal one of Penny's swords which Watts uses to hack into her.
After saying goodbye to Penny, the group flees to the Schnee Manor in order to hide and heal Nora. Upon arriving, they meet Whitley Schnee who reveals the staff abandoned the manor after Jacques's arrest. Weiss tells him to go to his room after tense conversation. The trio later watches Ruby's message to all of Remnant regarding Salem. Later, the group watches in horror as Salem using the Grimm Liquid from Monstra to break through Atlas's Dust Shields, landing the Grimm on the island, starting the Battle Of Atlas.
Weiss gets into an argument with May on defending either Atlas or Mantle. May prepares to leave for Mantle and tells Ruby, Weiss, and Blake about the situation where everyone cannot and must choose a side. The discussion ends when Klein Sieben shows up, having been called by Whitely to help Nora. Immediately after, Penny comes crashing down and apologizes before fainting.
The power in the manor goes off and the group decides to turn on the backup generator as suggest by both Klein and Willow Schnee who revels the location. While Weiss and Whitley go to Jacques's room to unlock his computer and prepare SDC Cargo Ships need to get Mantle refugees to safety, Ruby and Blake go to the backup generator and successfully turn back on the power. However the duo is then ambushed by The Hound who mistook Ruby for the Winter Maiden. Weiss rushes over after Blake calls to warn her, she and Blake tries to save a captured Ruby before the Grimm drops her upon realizing it got the wrong target.
While Weiss runs back into the Manor to save her family, Blake attempts to help Ruby only to get attack by an Cenitaur. Blake proceeds to battle the Grimm while begging Ruby to wake up, the latter wakes just in time to slay the Grimm before it can kill Blake. Meanwhile Nora calms down Penny who is being hacked by reminding her not to forget the rest of her while Weiss saves her family from The Hound. The group then witness The Hound knocking down a hacked Penny before Ruby uses her Silver Eyes to knock the beast out of the manor. However to the group's horror, not only does it survive but is reveled to have a Sliver-Eyed Faunus at its core. The trio are too scared to fight back but are saved when Willow and Whitley pushed an Armored Geist Statue onto the Hybrid, killing it. The group is is then left wondering what The Hound really was, as the Grimm's flesh disintegrates, leaving the host's skeleton behind.
Yang, Jaune, Ren, and Oscar later reunite with the rest of Ruby's Group alongside Emerald Sustrai. Later, their Scrolls go off and to their horror witness Ironwood's forces taking out some of the ships needed to get the people of Mantle to escape. Which is followed by him giving an ultimatum that either Penny opens the Atlas Vault or he will destroy Mantle completely using the bomb that was originally meant for Monstra.
When the group ends up arguing over how to handle the situation, Ruby ends up breaking down due to all the stress. Largely due to all of their previous plans not working out, and her belief that her Mother might have suffered the same fate as The Hound. When Yang talks to her about this, she tells her that they have all taken risks and that they aren't always going to work while helping her sister cope.
When Penny ends up being hacked again, the group try to stop her from leaving and try to restrain her with Emerald helping them. After Nora states that the hacked part of Penny is just a part of her, Jaune helps boost her Aura to let her fight against the virus but doesn't destroy it. The group believes that Penny going to the Vault is a risk that they haven't considered yet and seemingly agree to allow Penny to open the Vault for Ironwood. Although the group is unaware that Cinder and Watts were listening on their conversation.
In the end, they managed to defeat Ironwood and the Ace-Ops thanks to the help of Emerald, Winter, and Marrow and imprison him. The group heads to the Vault to help Penny before the virus overtakes her while also warning Atlas and Mantle that Atlas is about to fall before the broadcast is cut dead by Watts. Upon activating the Staff, the group ask Ambrosius to help them save Penny by granting her a Human body while keeping the virus in a copy of her original body, as well as and to create an doorway that will connect Atlas and Mantle to Vacuo.
When things seem to be working out for them, Cinder and Neo both appear and revealed that they already knew about their plans after they used the last question from the Relic of Knowledge. Neo attempts to kill Ruby, but Yang gets in between them and takes the hit meant for her sister and ends up falling into the void. When the evacuated people get to the other side of the portal, they end up caught in a sandstorm that attracts Grimm to their location while Ren, Emerald and Oscar fight after they realize that the portal is only one way and can't return.
During the ensuing fight, Penny is mortally wounded by Cinder and asks Jaune to kill her to ensure the powers cannot be taken by Cinder. After this, the rest of Team RWBY falls in due to Cinder's intervention, along with Neo who is betrayed at the last second by Cinder and Jaune who fails to make it through as the portals disappear.